Biodiversity and Stage of the Art of Three Pollinators Taxa in Mexico: An Overview

: The Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) confirmed that pollinators have declined in abundance and diversity; additionally, there is insufficient data for Latin America. Thus, we performed a review on scientific studies and databases to determine the state of the art of the diversity of three pollinator animals (bees, hummingbirds, and bats) in Mexico as well as an analysis of relevant public policies to conserve these species. We found 2063 bee species reported to be present in Mexico. The biodiversity of hummingbirds (58 species) and pollinator bats (12 species) is well known. We identified 57 scientific studies published in the last 20 years related to the biodiversity of bees (30 studies), hummingbirds (16 studies), and pollinator bats (11 studies). Relatively few, or no current studies on hummingbirds and pollinators bats at risk as well as for more than 1000 bee species is available. Great efforts have been made about policies and programs to improve the knowledge and conservation of pollinators in Mexico the last years such as the Species at Risk Conservation Program (PROCER), the Species Conservation Action Program (PACE), and the Natural Protected Ares System (CONANP). However, information of the status of many species and regions is still scarce. Thus, more studies about biodiversity, density, and trends as well as studies of the impact of policies and programs on pollinator species in Mexico are needed.


Introduction
Most cultivated and wild plants depend, at least in part, on animal vectors, known as pollinators. Although most animal pollinators are insects (for example, bees, flies, moths, and wasps), some vertebrate pollinators exist (for example, birds and bats) [1]. Pollinators are a key component of global biodiversity, maintenance of ecosystem health and function, wild plant reproduction, crop production, and food security [1][2][3]. These pollination services depend on both managed (for example, Apis mellifera and Bombus impatiens) and wild pollinators [4]. However, there is clear evidence of recent declines in both wild and managed pollinators, and the parallel declines in the plants and crops that rely upon them [1,5]. The potential drivers of pollinator loss, include habitat loss and fragmentation, agrochemicals, pathogens, alien species, and climate change [3].
The Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES), an independent intergovernmental body, was established by member States in 2012. The work program of IPBES includes assessing knowledge, policy support, building capacity and communications to identify and promote the scientific assessments about the planet's biodiversity, ecosystems, and the benefits they provide to people, as well as the development of policy instruments, tools, and methods to protect and sustainably use these vital natural resources [6]. The first global thematic assessment from IPBES in 2016, was the current state of knowledge about pollinators and pollination [4]. It confirmed that wild pollinators have declined in abundance and diversity in Northwest Europe and North America. Although an insufficiency of wild pollinator data (species, distribution, and abundance) for Latin America, Africa, Asia, and Oceania precludes any general statement on their regional status, local declines have been recorded. Long-term international or national monitoring of both pollinators and pollination is urgently required to provide information on status and trends for most species and most parts of the world [4].
Mexico, as an IPBES member, holds an exceptionally rich biodiversity ranking among the megadiverse countries of the word [7]. There are around 1800 species of butterflies and moths, more than 6000 species of bees, wasps, and ants, 58 species of hummingbirds, a dozen species of bats and several hundred species of beetles, that give a pollination service [8].
Nearly 85% of fruit and/or seed consumed species in Mexico depend to some degree on pollinators for productivity [9]. More than 90% of the leading global crop types are visited by bees [4]. Some hummingbird and bat species are important pollinators of food resources in Mexico, such as cactus fruits and agave species (including those used for tequila and mezcal) [4]. The conservation of these pollinators in Mexico is particularly important, not only for food safety but also for the conservation of biodiversity. Although the fauna of Mexico is most likely one of the best studied of Mesoamerica region, the diversity and status of many species is unknown [7]. Moreover, the last major studies related to the conservation status and diversity of species such as bees [10] and pollinating bats [11] were conducted more than 20 years ago.
The conservation of species depends largely on knowledge of their diversity, abundance, and distribution. All possible sources of data and information, including new, fastgrowing sources such as citizen science (for example, iNaturalist) and scientific studies are needed to improve the biodiversity conservation and monitoring [12].
To protect and sustainably use pollinators in Mexico, it is important to follow IPBES work program at the regional level. Therefore, the aim of this study was to review the biodiversity and conservation status of three pollinator animals (bees, hummingbirds, and bats) in Mexico, regarding to the complementary areas suggested for IPBES as follows: (1) to determine the diversity and the stage of the art of bees, hummingbirds, and pollinator bats in Mexico. (2) to analyze the relevant public policies related to biodiversity and conservation of pollinators in Mexico.

Materials and Methods
Methods for the literature search and collecting data are described.

Eligibility Criteria
Inclusion criteria. The study was performed in Mexico, focused on biodiversity of bees, hummingbirds, and pollinator bats, and published from January 2001 to October 2020. The study showed identification to species level. The study was written in English or Spanish.
Exclusion criteria. Studies dealing with production, reproductive biology, as well as reviews, or articles that mention pollinators but focused on the reproductive or herbivorous biology of plants were excluded.

Literature Search
The search was conducted on Google Scholar and PubMed databases. The search terms were: "biodiversity Mexico" or "pollination Mexico" followed by "bees" or "hummingbirds" or "pollinator bats". The timeframe was set from 2001 to 2020, the search was carried out on 30 October 2020. The search yielded 1774, 529, and 545 results for bees, hummingbirds, and pollinators bats, respectively (duplicates were removed; Figure 1).

Figure 1.
Study identification and screening following the PRISMA methodology.

Studies Selection
All sources were screened for potential inclusion in the review (on basis of tittle, abstract, and key words) and a total of 108, 34, and 37 studies were identified as potentially eligible for bees, hummingbirds, and pollinator bats, respectively ( Figure 1). The potentially eligible studies were evaluated to identify the studies for eligibility and a total of 30, 15, and 11 studies were included in the review after this step ( Figure 1).

Data Collection
To identify the status of diversity and policy support in Mexico, we performed a search on databases of government and private agencies with jurisdiction in biodiversity and conservation of pollinators.
We compiled a database of all species (bees, hummingbirds, and pollinators bats) reported in scientific studies and as well as species and occurrences recorded in iNaturalist (www.iNaturalist.com.mx; accessed on 31 October 2020), in the Global Biodiversity Information Facility (GBIF) [13] from January 2001 to October 2020. Only the occurrences classified as research grade by iNaturalist were included. The iNaturalist observations recorded in GBIF were discarded. The Integrated Taxonomic Information System (ITIS; www.itis.gov; accessed on 12 March 2021) was used to get valid taxonomy and synonyms.

Knowledge Assessment
Several studies have been conducted on the diversity of bees, hummingbirds, and pollinator bats in Mexico. In total we identified 57 scientific studies published in the last 20 years. The main topic was bees with 52.6% (30 studies), followed by hummingbirds with 28.1% (16 studies), and pollinator bats with 19.3% (11 studies; Figure 2A). In the last 5 years, the scientific contributions made on bats have decreased compared to previous years, while in the last years the contributions made on bees seem to be decreasing compared to the period 2012-2016 ( Figure 2B). The publications made on hummingbirds seem to be maintained ( Figure 2B). Most of the publications focused on bee biodiversity were carried out in the south, southeast, central west, and northeast regions of Mexico ( Figure 3); in the case of the northeast region, the studies were focused only on Nuevo Leon state ( Figure 3). Minckley [14] reported 383 bee species at San Bernardino Valley between Sonora Mexico and Arizona, USA; however, it was not mentioned the species found in Mexico; therefore, this study was not considered for this review. The studies performed on hummingbirds were focused on the Trans-Mexican Volcanic Belt in central Mexico ( Figure 3). Whereas the studies performed on pollinator bats were focused on central region. It is clear the need to perform studies in the regions where no studies have been carried out in the last 20 years, especially in the northwest and northeast region due to the richness of bee species in desert regions [10]. The web platform iNaturalist, is a global community that records observations of organisms and shares them in a database so that in collaboration with the National Commission for the Knowledge and Use of Biodiversity (CONABIO, Mexico) and specialists, they generate information and knowledge related to the identification and distribution of Mexican biodiversity. From January 2001 to October 2020 iNaturalist recorded 10,943, 22,227, and 286 observations of bees, hummingbirds, and pollinator bats, respectively (Table 1). These observations were classified as research grade by iNaturalist, which is the highest data quality assessment and may be used to establish hypothesis and perform studies about the biodiversity, distribution, and abundance of pollinator species. From January 2001 to October 2020 GBIF recorded 72,254, 309,109, and 2152 occurrences of bees, hummingbirds, and pollinator bats, respectively (Table 2). Citizen's science data, collected by collaborating volunteers and professional scientists are now widely used in biodiversity research, providing conservation information at a broad spatial and temporal scales relevant for policy making and management [12].

Bees
According to iNaturalist, GBIF, the National Information System on Biodiversity (SNIB-CONABIO) [15] and Discover Life [16] databases, 2063 bee species of 151 genera have been reported in Mexico (Supplement S1). However, just 502 species (Supplementary Table S1 ) were reported in scientific studies, 714 species were recorded in GBIF (Table 2), and 213 species were recorded in iNaturalist ( Table 1) the last 20 years; in total, 933 species were reported in Mexico from January 2001 to October 2020 (crossover between scientific studies, iNaturalist and GBIF information; Supplement S1). Therefore, relatively few, or no current information of more than 1000 bee species is available. Moreover, 850 species studied were reported as morphospecies (Supplementary Table S1), which means that more than 60% of the species reported were not completely identified. In the case of the observations recorded in iNaturalist, 8749 (44.4%) of them were reported as requiring ID (Table 1). Ayala et al. [10] mention that even with the increase of publications and specialist in bees, 56% of genus known in Mexico had not been reviewed. Inappropriate identification can limit the knowledge of the richness and decline of bees [47,48]. Although there have been described 126 new species in the last 20 years that occur in Mexico (Supplement S2), it is clear the need to establish a strategy to improve the identification of collected bees, as well as find out the conservation status of species that have not been studied or observed in the last 20 years.
In the last 20 years the bee genera Bombus and Apis were among the ones with more occurrences recorded in GBIF/iNaturalist ( Figure 4); these genera together with stingless bee species (less than 3% of total bee diversity) concentrated 47% of the occurrences recorded (Supplement S3). Some Bombus species have been considered as potential managed pollinators [49]. Globally, the pollinator that is predominantly managed to enhance agricultural production is Apis mellifera [1]. Both, wild and managed bees have a significant role in pollination [4] and the increase of the diversity of bee species can improve fruits production [50]. However, the pollination services provided by native species such as stingless bees can be more efficient than A. mellifera [51,52]. Moreover, it was observed that the introduction of non-native species can induce a disturbance on bee diversity due to an aggressive competitive behavior between species [34,53]. Therefore, it is important to perform more studies to evaluate the impact of the introduction of productive species on disturbance on bee diversity, as well as to promote the use of native stingless bee species (meliponiculture). The diversity and distribution of stingless bees present in Mexico is well known [54][55][56][57]. The genera Trigona and Scaptotrigona were among the ones with more occurrences recorded in GBIF/iNaturalist ( Figure 4). In Mexico, stingless bees represent a relatively small portion (2.6%) of the highly diverse bee fauna of the country, but the economic, tourism, social, and cultural impacts they have are of great importance [39,56,58]. They are considered among the major pollinators of many native and cultivated tropical plants [59,60]. Through the meliponiculture, the stingless bees could provide an important source of income for peasant farmers in areas where the use of Africanized honeybees is restricted and harnessing these bees to their full potential for honey and wax production [61]. According with SNIB-CONABIO [15] and Discover Life databases [16], 48 stingless bee species are present in Mexico (Supplement S1). The last review of stingless bees in Mexico reported 46 species of 16 genera [56]. The differences found between the sources suggest an improvement in the harmonization and updating between databases, and findings of publications. This pattern could be repeated for other bee species. Therefore, the 2063 bee species found in Mexico in our study should be a conservative estimate of the real bee biodiversity in Mexico due to outdated data, the unwell studied regions, and the unidentified species.

Hummingbirds
The diversity of hummingbird species in Mexico is well known [62,63]; 58 hummingbird species have been reported [63]. From January 2001 to October 2020, 44 species of 22 genera were reported in scientific studies (Table 3) and 58 species of 26 genera were recorded in iNaturalist and GBIF (Tables 1 and 2). Genera such as Abellia, Eupherusa, Florisuga, Heliothryx, Lophornis, Phaeochroa, and Thalurania were not mentioned or just mentioned by one study (Table 3) and they were between the less observed genera ( Figure 5).  Hummingbirds visit many wildflowers and pollinate many of them [81]. They also pollinate some cultivated plants that are important both ecologically and economically for humans, such as pineapples and cactus [82][83][84]. In addition to their ecological and economical importance, hummingbirds have always been important to human culture in Mesoamerica, representing gods, soul carriers, and fecundity among prehispanic societies, as well as good luck, love, and wellness, even in modern societies [85]. This may facilitate the recognition of these birds by people, which is reflected in the number of occurrences recorded in the last 20 years (Tables 1 and 2).

Pollinator Bats
Among mammals, bats are the principal pollinators [86]. Nectar-feeding bats (tribe Glossophagini) are an important component of the rich chiropteran fauna of Mexico [11]. They pollinate economically important plants such as agave and cactus to provide valuable products to humans, [87][88][89]. However, ecological attributes of glossophagines suggest that the species in this tribe such as Leptonycteris yerbabuenae, Leptonycteris nivalis and Choeronycteris mexicana might be more susceptible to extinction than other neotropical bats due to their dependence almost exclusively on nectar, pollen, and fruit they consume and their habitat loss where they obtain food [11].
In Mexico, 12 species of pollinator bats have been reported [11,15]. In the last 20 years, 7 species were reported in scientific studies (Table 4), the observation of 11 species was recorded in iNaturalist (Table 1) and the occurrence of 12 species was recorded in GBIF ( Table 2). Species such as Glossophaga commissarisi, Glossophaga leachii, Glossophaga morenoi, Hylonycteris underwoodi, Lichonycteris obscura have not been reported in scientific studies (Table 4) and they were between the less recorded species (Figure 6). The species Musonycteris harrisoni was the pollinator bat with fewest records in the last 20 years with only one record ( Figure 6).

Policy Support
IPBES suggest different strategies related to policy and management options to conserve and use the pollinators in a sustainable way such as reduce pesticide use, protect heritage sites and practices, translate pollinator research into agricultural practices, support knowledge co-production and exchange among indigenous and scientists, and support innovative pollinator activities that engage stakeholders [4]. In Mexico there are several programs and systems to know and conserve the biodiversity of species, such as the SNIB-CONABIO, the Species at Risk Conservation Program (PROCER), the Species Conservation Action Program (PACE), and the Natural Protected Ares System (CONANP) [101]. The CONANP comprises 182 areas and 90,839,521 ha of the country's territory that includes biosphere reserves, national monuments, national parks, as well as other state protected areas [101]. Bees, hummingbirds, and pollinator bats have been studied in these protected areas [21,24,63,64,67,79,102,103]. Other pollinators species such as moths (family Sphingidae) [94], flies (family Syrphidae) [104], and wasps (subfamily Polistinae) [94] were also found in these protected areas. These studies have made local efforts to increase the knowledge of pollinators, however, there is currently no national research project to study pollinators in these protected areas. Moreover, more areas should be included in the national system of protected areas to ensure the conservation of endemic species [63,97]. Different Government strategies have been implemented in Mexico to involve the society in the conservation of pollinator species such as digital platforms (www.iNaturalist.com.mx; www.enciclovida.mx; www.ebird.org; accessed on 31 October 2020) and the construction of gardens for pollinators [8]. However, there are no studies evaluating the impact of current programs, strategies, and policies on the population trends of pollinator species.
The CONABIO was created in 1992 to promote, coordinate, support, and carry out activities aimed to the knowledge, conservation, and sustainable use of biodiversity for the benefit of society of Mexico [8]. As a result, the Mexican Official Norm NOM-059-SEMARNAT-2010 about the environmental protection-native Mexican wildlife species with a list of species at risk was published [105]. Among the species at risk registered by norm, there are 4 pollinator bats species and 20 hummingbird species in different risk categories ( Table 5). The bat Musonycteris harrisoni and the hummingbirds Doricha eliza, Eupherusa cyanophrys and Lophornis brachylophus are categorized as endangered, they have few observations in the last 20 years, and according to the International Union for Conservation of Nature (IUCN) their population trends are decreasing (Table 5). Special mention is made on the hummingbird Hylocharis eliciae, which although not listed as at risk by NOM-059-SEMARNAT-2010 or the IUCN, was recorded only 85 times in GBIF/iNaturalist the last 20 years. On the other hand, 11 Bombus species that occur in Mexico are categorized at risk by the IUNC [106]; however, no bee species are considered within the list of the NOM-059-SEMARNAT-2010. Table 5. List of pollinator species at risk by Mexican laws (NOM-059-SEMARNAT-2010) [104] and their conservation status. threatened; LC, least concern. * Data from IUCN [106]. ** GBIF/iNaturalist occurrences reported in Mexico from January 2001 to October 2020.
Although there is an overall agreement about the pollinators decline, there are not wild pollinator data for many countries [4], and well documented cases are rare [47]. Our findings showed that there is an underestimation of bee diversity and a large number of bee species have not been studied or observed in the last 20 years. The information on hummingbirds, and pollinator bats diversity in Mexico seem to be more detailed. However, special attention should be paid on hummingbirds and pollinator bats at risk due to the few information and observations in the last years. IPBES mentions the importance of monitoring pollinator species to provide information on status and trends for most species [4]. Therefore, more studies are needed to know the biodiversity, abundance, and trends of bees, hummingbirds, and pollinator bats in Mexico. The knowledge of the status and biodiversity of pollinators species that inhabit Mexico will contribute to make policies and programs for their conservation.
In 2019, the Secretariat of Agriculture and Rural Development (AGRICULTURA) and Secretariat of the Environment and Natural Resources (SEMARNAT) of Mexico formalized the setup of the Coordination Group for the Preservation and Sustainable Use of Pollinators. The measure considers the creation of a national strategy in conjunction with the government, academic, research institutions, producers, and entrepreneurs with the aim to get a realistic diagnosis of the causes for the reduction in the pollinators' population as well as promote research to find new alternatives for the protection of these species [107]. This strategy is considered to start in the next years and together with the growing interest in meliponiculture, tequila and mezcal production, it could be an opportunity to improve the knowledge and conservation status of pollinators species in Mexico.

Conclusions
The biodiversity of hummingbirds and pollinator bats is well known but still unknown for bees. We show a list of bee species that occur in Mexico, but it should be a conservative estimate of the real bee biodiversity due to outdated data, the unwell studied regions, and the unidentified species. Relatively few, or no current information of more than 1000 bee species is available. Although great efforts and policies have been made for the biodiversity knowledge and conservation of bees, hummingbirds, and pollinating bats in Mexico the last years, the information and occurrences recorded of many species and regions are still scarce, especially in species at risk. Therefore, the findings of this review might be used to explore further studies on the status of pollinator species with relatively few, or no current information. Moreover, studies of the impact of policies and programs on pollinator species in Mexico are needed.